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Patterned Anchorage to the Apical Extracellular Matrix Defines Tissue Shape in the Developing Appendages of Drosophila.

Ray RP, Matamoro-Vidal A, Ribeiro PS, Tapon N, Houle D, Salazar-Ciudad I, Thompson BJ - Dev. Cell (2015)

Bottom Line: Here, we describe a genetic pathway that shapes appendages in Drosophila by defining the pattern of global tensile forces in the tissue.Altering Dp expression in the developing wing results in predictable changes in wing shape that can be simulated by a computational model that incorporates only tissue contraction and localized anchorage.Three other wing shape genes, narrow, tapered, and lanceolate, encode components of a pathway that modulates Dp distribution in the wing to refine the global force pattern and thus wing shape.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK; The Francis Crick Institute, Lincoln's Inn Fields Laboratory, 44 Lincoln's Inn Fields, London WC2A 3PX, UK. Electronic address: robert.ray@crick.ac.uk.

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Altering the Pattern of Dp Gives Rise to Predictable Changes in Wing Shape(A–E) Adult wing phenotypes for wild-type (A), localized silencing of Dp with dpp-Gal4 (B), sal-Gal4 (C), brk-Gal4 (D), hh-Gal4 (E) (top), diagrams showing the region of the wing where Dp is silenced (green), and the corresponding pattern of Dp anchorage (red asterisks) (bottom).(F–J) Developmental time course of pupal wing development revealed by phalloidin staining (red) showing the ontogeny of the shape change from 18 to 24 hr APF. The position of the pupal cuticle with respect to the wing is shown in the final panel (dashed white line).(K–O) The final images from the computational simulations of the genotypes corresponding to (A)–(E), using the epithelial vertex model (see Movie S2). The wing blade cells are shaded red, the hinge cells are shaded light blue, and the vein cells are shaded dark blue. The dashed white lines mark the wing outline at the beginning of the simulation. The Dp anchorage to the cuticle is shown as green lines ending with green dots and the anchorage in the hinge as green dots.
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fig4: Altering the Pattern of Dp Gives Rise to Predictable Changes in Wing Shape(A–E) Adult wing phenotypes for wild-type (A), localized silencing of Dp with dpp-Gal4 (B), sal-Gal4 (C), brk-Gal4 (D), hh-Gal4 (E) (top), diagrams showing the region of the wing where Dp is silenced (green), and the corresponding pattern of Dp anchorage (red asterisks) (bottom).(F–J) Developmental time course of pupal wing development revealed by phalloidin staining (red) showing the ontogeny of the shape change from 18 to 24 hr APF. The position of the pupal cuticle with respect to the wing is shown in the final panel (dashed white line).(K–O) The final images from the computational simulations of the genotypes corresponding to (A)–(E), using the epithelial vertex model (see Movie S2). The wing blade cells are shaded red, the hinge cells are shaded light blue, and the vein cells are shaded dark blue. The dashed white lines mark the wing outline at the beginning of the simulation. The Dp anchorage to the cuticle is shown as green lines ending with green dots and the anchorage in the hinge as green dots.

Mentions: If the localization of Dp determines tissue shape during hinge contraction, then changing the pattern of Dp localization in the wing should result in predictable changes in shape. To test this, we silenced dp in defined patterns in the wing with the drivers dpp-Gal4, sal-Gal4, brk-Gal4, and hh-Gal4, thus generating novel patterns of dp anchorage (Figures 4A–4J). Knockdown of dp in the intervein between L3 and L4 with dpp-Gal4 results in a retraction of the distal tip of the wing, where this intervein intersects with the margin (Figures 4B and 4G). A similar retraction of the distal tip of the wing is seen with sal-Gal4>dp-RNAi, but the phenotype is more severe, reflecting the broader expression of the driver (Figures 4C and 4H). Notably, this phenotype is similar to the dumpy phenotype associated with classical dp alleles (Figure 1C). RNAi depletion of dp in the complementary pattern with brk-Gal4 results in a narrowing of the wing blade consistent with loss of anchorage along the anterior and posterior margins (Figures 4D and 4I), whereas silencing dp in the posterior compartment with hh-Gal4 results in a contraction of the posterior part of the blade (Figures 4E and 4J). To address whether these phenotypes can arise as a result of alterations in the anchorage of the tissue, we incorporated the predicted patterns of Dp from each of our experiments into our computer model. The resulting simulated wing shapes resemble the corresponding in vivo phenotypes (Figures 4K–4O and Movie S2). These results indicate that the pattern of Dp attachment, coupled with contraction of the tissue, can account for the wing shape phenotypes observed in vivo.


Patterned Anchorage to the Apical Extracellular Matrix Defines Tissue Shape in the Developing Appendages of Drosophila.

Ray RP, Matamoro-Vidal A, Ribeiro PS, Tapon N, Houle D, Salazar-Ciudad I, Thompson BJ - Dev. Cell (2015)

Altering the Pattern of Dp Gives Rise to Predictable Changes in Wing Shape(A–E) Adult wing phenotypes for wild-type (A), localized silencing of Dp with dpp-Gal4 (B), sal-Gal4 (C), brk-Gal4 (D), hh-Gal4 (E) (top), diagrams showing the region of the wing where Dp is silenced (green), and the corresponding pattern of Dp anchorage (red asterisks) (bottom).(F–J) Developmental time course of pupal wing development revealed by phalloidin staining (red) showing the ontogeny of the shape change from 18 to 24 hr APF. The position of the pupal cuticle with respect to the wing is shown in the final panel (dashed white line).(K–O) The final images from the computational simulations of the genotypes corresponding to (A)–(E), using the epithelial vertex model (see Movie S2). The wing blade cells are shaded red, the hinge cells are shaded light blue, and the vein cells are shaded dark blue. The dashed white lines mark the wing outline at the beginning of the simulation. The Dp anchorage to the cuticle is shown as green lines ending with green dots and the anchorage in the hinge as green dots.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4539345&req=5

fig4: Altering the Pattern of Dp Gives Rise to Predictable Changes in Wing Shape(A–E) Adult wing phenotypes for wild-type (A), localized silencing of Dp with dpp-Gal4 (B), sal-Gal4 (C), brk-Gal4 (D), hh-Gal4 (E) (top), diagrams showing the region of the wing where Dp is silenced (green), and the corresponding pattern of Dp anchorage (red asterisks) (bottom).(F–J) Developmental time course of pupal wing development revealed by phalloidin staining (red) showing the ontogeny of the shape change from 18 to 24 hr APF. The position of the pupal cuticle with respect to the wing is shown in the final panel (dashed white line).(K–O) The final images from the computational simulations of the genotypes corresponding to (A)–(E), using the epithelial vertex model (see Movie S2). The wing blade cells are shaded red, the hinge cells are shaded light blue, and the vein cells are shaded dark blue. The dashed white lines mark the wing outline at the beginning of the simulation. The Dp anchorage to the cuticle is shown as green lines ending with green dots and the anchorage in the hinge as green dots.
Mentions: If the localization of Dp determines tissue shape during hinge contraction, then changing the pattern of Dp localization in the wing should result in predictable changes in shape. To test this, we silenced dp in defined patterns in the wing with the drivers dpp-Gal4, sal-Gal4, brk-Gal4, and hh-Gal4, thus generating novel patterns of dp anchorage (Figures 4A–4J). Knockdown of dp in the intervein between L3 and L4 with dpp-Gal4 results in a retraction of the distal tip of the wing, where this intervein intersects with the margin (Figures 4B and 4G). A similar retraction of the distal tip of the wing is seen with sal-Gal4>dp-RNAi, but the phenotype is more severe, reflecting the broader expression of the driver (Figures 4C and 4H). Notably, this phenotype is similar to the dumpy phenotype associated with classical dp alleles (Figure 1C). RNAi depletion of dp in the complementary pattern with brk-Gal4 results in a narrowing of the wing blade consistent with loss of anchorage along the anterior and posterior margins (Figures 4D and 4I), whereas silencing dp in the posterior compartment with hh-Gal4 results in a contraction of the posterior part of the blade (Figures 4E and 4J). To address whether these phenotypes can arise as a result of alterations in the anchorage of the tissue, we incorporated the predicted patterns of Dp from each of our experiments into our computer model. The resulting simulated wing shapes resemble the corresponding in vivo phenotypes (Figures 4K–4O and Movie S2). These results indicate that the pattern of Dp attachment, coupled with contraction of the tissue, can account for the wing shape phenotypes observed in vivo.

Bottom Line: Here, we describe a genetic pathway that shapes appendages in Drosophila by defining the pattern of global tensile forces in the tissue.Altering Dp expression in the developing wing results in predictable changes in wing shape that can be simulated by a computational model that incorporates only tissue contraction and localized anchorage.Three other wing shape genes, narrow, tapered, and lanceolate, encode components of a pathway that modulates Dp distribution in the wing to refine the global force pattern and thus wing shape.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK; The Francis Crick Institute, Lincoln's Inn Fields Laboratory, 44 Lincoln's Inn Fields, London WC2A 3PX, UK. Electronic address: robert.ray@crick.ac.uk.

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Related in: MedlinePlus